Converging intracortical signatures of two separated processing timescales in human early auditory cortex

Neural oscillations in auditory cortex are argued to support parsing and representing speech constituents at their corresponding temporal scales. Yet, how incoming sensory information interacts with ongoing spontaneous brain activity, what features of the neuronal microcircuitry underlie spontaneous and stimulus-evoked spectral fingerprints, and what these fingerprints entail for stimulus encoding, remain largely open questions. We used a combination of human invasive electrophysiology, computational modeling and decoding techniques to assess the information encoding properties of brain activity and to relate them to a plausible underlying neuronal microarchitecture. We analyzed intracortical auditory EEG activity from 10 patients while they were listening to short sentences. Pre-stimulus neural activity in early auditory cortical regions often exhibited power spectra with a shoulder in the delta range and a small bump in the beta range. Speech decreased power in the beta range, and increased power in the delta-theta and gamma ranges. Using multivariate machine learning techniques, we assessed the spectral profile of information content for two aspects of speech processing: detection and discrimination. We obtained better phase than power information decoding, and a bimodal spectral profile of information content with better decoding at low (delta-theta) and high (gamma) frequencies than at intermediate (beta) frequencies. These experimental data were reproduced by a simple rate model made of two subnetworks with different timescales, each composed of coupled excitatory and inhibitory units, and connected via a negative feedback loop. Modeling and experimental results were similar in terms of pre-stimulus spectral profile (except for the iEEG beta bump), spectral modulations with speech, and spectral profile of information content. Altogether, we provide converging evidence from both univariate spectral analysis and decoding approaches for a dual timescale processing infrastructure in human auditory cortex, and show that it is consistent with the dynamics of a simple rate model.Author summaryLike most animal vocalizations, speech results from a pseudo-rhythmic process that reflects the convergence of motor and auditory neural substrates and the natural resonance properties of the vocal apparatus towards efficient communication. Here, we leverage the excellent temporal and spatial resolution of intracranial EEG to demonstrate that neural activity in human early auditory cortical areas during speech perception exhibits a dual-scale spectral profile of power changes, with speech increasing power in low (delta-theta) and high (gamma - high-gamma) frequency ranges, while decreasing power in intermediate (alpha-beta) frequencies. Single-trial multivariate decoding also resulted in a bimodal spectral profile of information content, with better decoding at low and high frequencies than at intermediate ones. From both spectral and informational perspectives, these patterns are consistent with the activity of a relatively simple computational model comprising two reciprocally connected excitatory/inhibitory sub-networks operating at different (low and high) timescales. By combining experimental, decoding and modeling approaches, we provide consistent evidence for the existence, information coding value and underlying neuronal architecture of dual timescale processing in human auditory cortex.